ABSTRACT. The food relocation and nesting behavior of the South American genus Eucranium Brullé is described based on observations carried out under natural conditions. Food preference, food transportation, period of surface activity, and habitat preference are described for two species, E. arachnoides Brullé and E. planicolle Burmeister. The biology and food relocation behavior of Eucranium is compared with that of the morphologically similar South African subgenus Scarabaeus (Pachysoma) MacLeay. The convergent adaptations to psamophilous habitats of Eucranium and S. (Pachysoma) are discussed.

The genus Eucranium Brullé is a relatively small genus of dung beetles belonging to the Eucraniini (Coleoptera, Scarabaeidae), a morphologically and behaviorally unique New World tribe endemic to the Chaqueña and Monte Biogeographic provinces in Argentina (Zunino et al., 1991; Philips et al., 2002). Members of the Eucraniini are unusual in that they occur only in specific thorn-desert habitats and have very specialized ecological adaptations (Ocampo, 2004, 2005). Unusual behaviors include excavating burrows before foraging and feeding on dry dung, traits once thought limited to the southwest African subgenus Scarabaeus (Pachysoma) MacLeay. Presently, the tribe Eucraniini consists of four genera: Anomiopsoides Blackwelder (five species) (Ocampo, 2005), Ennearabdus van Lansberge (one species), Eucranium Brullé (seven species) (Ocampo, in prep.), and Glyphoderus Westwood (three species) (Ocampo, 2004).

The taxonomic placement of the tribe has been enigmatic due to their unusual biology and external morphology. Recently it was hypothesized that Eucraniini is a monophyletic group related to the Phanaeini with both derived from Dichotomiini (Philips et al., 2002; 2004; Ocampo et al., in prep.). The species-level taxonomy of the genus Eucranium has been enigmatic; seven species were recognized for this genus, but probably, based on an ongoing revision, the genus consists on more species (Ocampo, in prep.).

The genus Eucranium is restricted to the Monte and Chacoan biogeographic provinces in Argentina from 26°-43° latitude South and between 200-2,800 m elevation (Roig Juñent and Flores, personal communication). The climate in this area is temperate-arid with little rainfall (80-250 mm per year) (Roig-Juñent et al., 2001). The northern and central regions of the Monte and southern portion of the Chacoan province receive rain in summer, but in the south it is colder and rainfall is distributed throughout the year (Morello, 1958; Cabrera, 1976). The dominant vegetation of this region is open scrubland (Figs. 1-2). The landscape consists of sandy plains and plateaus and is characterized by the presence of mountains that define several elongated valleys. All species studied prefer sandy, or clay soils with a 20-60% vegetation cover.

Species of Eucranium and S. (Pachysoma) are morphologically similar, having undergone convergent adaptations for survival in xeric habitats. Both taxa have completely different modes of transporting dung, which is an indication of the descent of each from two unrelated lineages within the Scarabaeinae.

This paper is a continuation of our work on the taxonomy and evolution of the food relocation and nesting behavior of the genera of Eucraniini. The aim of this paper is to provide a qualitative description of the behavior of the species of Eucranium and to compare it to the species in the southwestern African S. (Pachysoma). Images and videos on the food relocation behavior and natural history of the tribe Eucraniini are available on the World Wide Web page at http://www.museum.unl.edu/research/entomology/Eucraniini/Eucraniini1.html.

METHODS

Observations on the biology and food relocation behavior of two species of Eucranium,E. arachnoides Brullé and E. planicolle Burmeister were carried out under natural conditions in Mendoza, La Rioja, and Neuquén provinces, Argentina (Mendoza: Reserva Telteca, Reserva Provincial La Payunia, and Pata Mora; La Rioja: Anillaco), for a period of ten days in January 2002 and seven days in January 2003. During our observations, air temperature varied from 18 to 38 °C in the shade, with the hottest temperature recorded at 13:00-15:00 hr and the coolest temperature at night.

Food relocation and nesting behavior of Eucranium Brullé

Under natural conditions, the period of surface activity of E. arachnoides and E. planicolle is from 10:00-13:00 hr, and from 18:00-20:00 hr, depending on the air and soil temperatures. Nocturnal surface activity was observed for E. arachnoides in Reserva Talteca, Mendoza from 22:00-23:30 hr. Nocturnal activities of E. arachnoides consisted of walking in an apparently random manner in what we presume is a search for mates, because no beetles were observed carrying dung or walking rapidly (speed may be temperature dependent) like they do when foraging in the daylight and several individuals were observed sitting on the sand with their antennal club open. Eucranium species, as in most other members of the Eucraniini, specialize trophically on dehydrated dung pellets. Individuals of E. arachnoides and E. planicolle were observed carrying pellets of "goat" (Capra hircus L.), and E. planicolle was observed carrying pellets of "guanaco" (Lama guanicoe Cuvier). Eucranium arachnoides and E. planicolle were also observed using dry horse or cow dung (Fig. 3) but they were not attracted to dung traps baited with fresh human or cow dung. Generally, Eucranium species are not found directly associated with rodent nests, which is often the case in the other two flightless genera of Eucraniini, Anomiopsoides and Glyphoderus. One of us (Ocampo) observed an association of Eucranium arachnoides with a guanaco dung midden in Mendoza province. To carry dung, the beetles grasp it with the foretibiae and run forward using only their middle and hind legs (Fig. 3). This unique behavior is known only for members of the tribe Eucraniini.

One species, E. arachnoides, was also observed moving a large piece of horse dung by butting it. To do this, the beetles used their forelegs and head to push dung while walking forward. Sometimes after several unsuccessful attempts to transport a large piece to their burrow, the beetle decided to dig a new burrow, then fragmented the piece of dung by using the clypeus and forelegs, and then buried it. The method of food relocation by butting the dung piece was also observed in the Eucraniini Ennearabdus lobochephalus (Harold) (Ocampo, personal observation), in various species of Phanaeus MacLeay (Phanaeini), and in Dichotomius nisus (Olivier) (Dichotomiini) (Halffter & Matthews, 1966; Halffter & Edmonds, 1982). Species that also carry food with their front legs are found in the Australian genus Cephalodesmius Westwood. In contrast though, Cephalodesmius species walk backwards while holding food and gather fresher and moister food particles, such as leaves and flowers, in its humid forest habitat (Monteith & Storey, 1981). Coptorhina Hope is another genus that has been recorded carrying food (mushroom pieces) with its front legs while moving backwards (Tribe, 1976).

When the entrance of the burrow is reached, the observed specimens of E. arachnoides and E. planicolle entered by walking forward rather than backward. Observations published by Zunino et al. (1989) suggested that the beetles drop the dung pellet and turn back and enter the nest walking backward while dragging the pellet. We never observed this for Eucraniini species under natural conditions (see Ocampo, 2004, in press) but one of us (Philips) observed this alternative behavior under laboratory conditions. The burrow is always dug prior to provisioning. It is variable in depth (usually between 0.2-0.8 m long) and variable in slope (between 35-60° with respect to the ground surface). The tunnel may be straight or curved. The depth of the burrow is probably associated with the depth where beetles find a certain level of soil moisture. Burrows are sometimes bifurcated near the end and in those cases only one chamber was observed provisioned with dung. Beetles store the food at the end of the burrow, and no special chamber was prepared for it. The number of dung pellets or dung pieces found stored is variable, and ranges from three to 193 for E. arachnoides, each pellet is carried independently to the burrow. Sexual cooperation has been observed, and it follows the same behavior as that for individuals. Occasional vigilance at the entrance of the burrow was noted and this is done by one of the members of the couple. No special brood chambers were observed in burrows constructed by pairs. During the hours with no surface activity, it is common to observe the entrance of the burrow obscured with sand or other substrate.

Comparison with the South African flightless Scarabaeus (Pachysoma)

Species of the subgenus Scarabaeus (Pachysoma) MacLeay are found only in southwest Africa and range from Cape Town, South Africa, north to near Walvis Bay, Namibia from approximately 34º to 23º S latitude (Harrison & Philips, 2003). They are found along coastal sands from near sea level to approximately 1,500 m in altitude (near Aus, Namibia). Species are distributed in the predominantly winter rainfall areas where at least 2/3 of the precipitation occurs during this cooler season (Goldblatt, 1978). The amount of rainfall varies from 400-500 mm in the lowland southwest Cape region decreasing to no more than 100 mm per annum in the Namib Desert.

Thirteen species are now included in the subgenus (Harrison et al., 2003). Similar to Eucranium,S.(Pachysoma) is a denizen of areas with sandy soils. The vegetation density in their habitat ranges from bare loose sand dunes to firmer sandy-gravel areas (mainly in Namibia) to vegetated scrub landscapes of varying sand firmness in Namaqualand to the Cape region in South Africa. The habitat varies from flat to various undulating topologies, such as river banks and dry beds, coastal hummocks, and vegetated dunes (Harrison et al., 2003; Philips, personal observation).

The peculiar foraging behavior for S. (Pachysoma) was first recorded by Holm & Scholtz (1979). Species of S. (Pachysoma) use their posterior legs to grasp either dung or detritus, depending upon the species, in a pincher-like manner. Individuals walk forwards dragging food to burrows. In a slight variation, S. (Pachysoma)denticollis (Péringuey) reportedly picks up detritus with its hind legs and presses this material against the ventral abdominal surface (Holm & Scholtz, 1979). In contrast, species of Eucranium use their front legs to hold food, which is often held well above the ground surface while they transport it.

Foraging behavior of S. (Pachysoma)striatum (Castelnau) was recorded by Scholtz (1989). He found that beetles are active on the surface from 9:00-18:00 hr with the most intense activity from 10:00-12:00 hr and 15:00-17:00 hr. Temporary burrows were sometimes excavated at midday and also in mid-afternoon when the temperature was decreasing. Harrison et al. (2003) noted foraging of S. (Pachysoma)aesculapius Olivier as occurring slightly earlier (ca. 7:00-9:00 hr) and slightly later (ca. 16:00-18:00 hr) than the previous species. Except for the earlier activity of S. (Pachysoma)aesculapius, activity periods are similar to Eucranium and nocturnal activity is not known in S. (Pachysoma) species.

Three species of S. (Pachysoma) have been observed in what appears to be pheromone releasing behavior at the burrow entrance (Harrison et al., 2003). This has not been observed in any Eucraniini. The degree of sexual cooperation, if any, is unknown. Scholtz (1989) reported only one burrow out of 21 for S. (Pachysoma)striatum had an individual of each sex. Based on field work with several other species, finding two individuals (of unknown sex) in a single burrow was even less common (Philips, personal observation).

Like in Eucranium species, the burrow was always excavated before gathering dung. It was dug at a angle of about 45° to the surface and variable in depth with a total length of 45-60 cm. The burrow usually had several abrupt turns on the way down to the dung chamber (Scholtz, 1989; Philips, personal observation). As in Eucranium, the depth of the burrow was apparently associated with a certain level of soil moisture that is sometimes manifested as a distinct damp zone horizon below dry sand. In contrast to Eucranium species, but like many other Scarabaeini (see Halffter & Matthews, 1966), S. (Pachysoma) species excavate dung chambers. The first chamber excavated is for temporary storage, while a second, deeper chamber below the moisture line, was where feeding and brood rearing apparently occurred. As in Eucranium, the number of dung pellets or the amount of detritus stored is variable and pellets are carried one by one into the burrow. Based on 14 burrows, Scholtz (1989) found an average mass of 1.4 g of air-dried rodent dung (range=0.53-2.57 g). Once sufficient dung was collected, burrow entrances were blocked with sand pushed up to the entrance by the inhabitant.

As with Eucranium species, fresh wet dung was not very attractive to S. (Pachysoma) species and would be ignored until it partially dried out (Scholtz, 1989). Native dung used as food included that of many rodent species (Scholtz, 1989), oryx or gemsbok (Oryx gazella L.), species of S. (Pachysoma) have also been observed utilizing sheep and hare pellets, ostrich dung, dead insects, and mice and chameleon droppings (Holm, 1970; Holm & Scholtz, 1979). It is likely that dung from the Greater Kudu (Tragelaphus strepsiceros Pallas), Grey Duiker (Sylvicapra grimmia L.), Springbok (Antidorcas marsupialis Zimmermann), Zebra (Equus zebra L.), and undoubtedly many other small antelope species could also be utilized as a food resource. Like Eucranium species, there is no evidence that Pachysoma species were associateed with rodent nests.

Some species of Pachysoma, such as S. (Pachysoma)hippocrates (MacLeay) and S. (Pachysoma)glentoni Harrison, Scholtz, and Chown feed on detritus, although the former will feed on dung if available. Six of seven excavated nests of S. (Pachysoma)endroedyi Harrison, Scholtz, and Chown were found to contain a combination of detritus and pellets, eight of 17 nests of S. (Pachysoma)gariepinus (Ferreira) contained only detritus or a mixture of detritus and dung, and the single excavated nest of S. (Pachysoma)bennigseni (Felsche) contained a mixture. Scarabaeus (Pachysoma)schinzi (Fairmaire) is known to feed on vegetable matter (Harrison et al., 2003) and dung (Philips, personal observation). Although Eucranium species are known to use dung only, there are at least two species of the closely related genus Anomiopsoides that also use detritus, seeds, and other plant material as food (Ocampo, in press).

Larvae of S. (Pachysoma) are reported for two species (Harrison et al., 2003). There is no use of a brood pear or ball of dung, and the larvae appear to be open-nest feeders as they lack the characteristic dorsal hump found in other ball-confined larvae. Lack of a brood ball is also appears true in lab colonies of Eucranium. In the closely related Anomiopsoides, pupae in lab colonies were enclosed in cells composed of organic material and sand. In contrast, S. (Pachysoma) species are known to pupate in fragile sand cases.

Populations of S. (Pachysoma) vary in density that is perhaps dependent upon the amount of available dung and the harshness of the environmental conditions (Philips, personal observation). Unfortunately, there is little available data to substantiate the sizes and densities of populations, and false impressions may be created due to the degree of above-ground or tunneling activity observed. It is apparent that most dung is encountered by chance and, at least for some populations, is plentiful and not limiting to population size (Scholtz, 1989). Additionally, interspecific competition (within the subfamily Scarabaeinae) is reduced or even lacking because most other scarabaeines are not attracted to dry dung. It is possible that reduced amounts of dung for nesting in some habitats may have been the selective force improving the fitness of those individuals that use detritus.

It is not clear how beetles find their way back to the burrow along the shortest possible route. As described by Byrne et al. (2003) and Dacke & Warrant (2002) for the South African winged dung beetles Scarabaeus rugosus (Hausman), S. rusticus (Boheman), Kheper nigroaeneus (Boheman) and Pachylomerus femoralis (Kirby) (Scarabaeinae: Scarabaeini), and suggested for the Eucraniini genera Anomiopsoides and Glyphoderus (Ocampo, 2004), the beetles rely on the pattern of polarized light as a compass bearing that can be used to "calculate" the direction to the burrow. Dacke et al. (2003) documented the use of polarized moonlight by the African Scarabaeus zambesianus Péringuey that forages at night for fresh dung. We cannot infer the same adaptation for E. arachnoides, since observations of nocturnal activity of this species were conducted during the dark phase of the moon (Ocampo personal observation).

Species of Eucranium and S. (Pachysoma) are dry dung (or dry detritus) feeders. Scarabaeus species formerly placed in the genus Mnematium MacLeay and Neomnematium Janssens, (S. silenus (Grey), S. ritchiei (MacLeay), and S. cancer (Arrow)) may also have similar food feeding and relocation strategies of dragging or carrying as evidenced by common ancestry (Harrison & Philips, 2003). Unfortunately, there is no information available on the feeding habits of these species although their mouthpart structure appears to be intermediate between wet dung and dry dung feeders (Harrison et al., 2003).

ACKNOWLEDGMENTS

We thank Brett Ratcliffe and Mary Liz Jameson (University of Nebraska, Lincoln) for their critical review of the manuscript and valuable comments. We also thank Sergio Roig-Juñent, Gustavo Flores, and Guillermo Debandi (Instituto de Investigaciones de Zonas Áridas, Mendoza, Argentina) for their help and logistical support during field trips in Argentina in January 2002 and 2003, and to David Gorla (Centro Regional de Investigaciones Científicas y Transferencia Tecnológica, La Rioja, Argentina) for his help and hospitality during our field trip in Argentina in January 2002. Our appreciation also to Ogden College and the Department of Biology, Western Kentucky University, for supporting travel in Argentina for Philips. A University of Pretoria Post-doctoral Fellowship enabled field observations of S. (Pachysoma) species in both Namibia and South Africa. We thank the Dirección de Recursos Naturales Renovables de la provincia de Mendoza for letting us to conduct our studies in Reserva Provincial Telteca and Reserva Provincial Payunia. Lastly, this project was supported by an NSF/PEET grant (DEB-0118669) to Mary Liz Jameson and Brett Ratcliffe, by an NSF Biotic Surveys and Inventory grant (DEB-9870202) to Brett Ratcliffe and Ronald Cave, a NSF Biotic Surveys and Inventory grant (DEB-0342189) to Andrew Smith and Federico Ocampo and by a Graduate Student Research Support Award from the Initiative for Ecological and Evolutionary Analysis (IEEA) at the University of Nebraska to Federico Ocampo.